The phylogeography and ecology of oligobrachia frenulate species suggest a generalist chemosynthesis-based fauna in the arctic

We used ancient DNA (aDNA) extraction methods to sequence museum voucher samples of Oligobrachia webbi, a frenulate siboglinid polychaete described from a northern Norwegian fjord over fifty years ago. Our sequencing results indicate a genetic match with the cryptic seep species, Oligobrachia haakon...

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Published in:Heliyon
Main Authors: Sen, Arunima, Andersen, Liselotte W., Kjeldsen, Kasper U., Michel, Loïc, Hong, Wei Li, Choquet, Marvin, Rasmussen, Tine L.
Other Authors: Biologie des Organismes et Ecosystèmes Aquatiques (BOREA), Université de Caen Normandie (UNICAEN), Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA), Biologie et Ecologie des Ecosystèmes Marins Profonds (BEEP), Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2023
Subjects:
Online Access:https://hal.science/hal-04204000
https://doi.org/10.1016/j.heliyon.2023.e14232
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spelling ftccsdartic:oai:HAL:hal-04204000v1 2024-02-27T08:37:07+00:00 The phylogeography and ecology of oligobrachia frenulate species suggest a generalist chemosynthesis-based fauna in the arctic Sen, Arunima Andersen, Liselotte W. Kjeldsen, Kasper U. Michel, Loïc Hong, Wei Li Choquet, Marvin Rasmussen, Tine L. Biologie des Organismes et Ecosystèmes Aquatiques (BOREA) Université de Caen Normandie (UNICAEN) Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA) Biologie et Ecologie des Ecosystèmes Marins Profonds (BEEP) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS) 2023-03 https://hal.science/hal-04204000 https://doi.org/10.1016/j.heliyon.2023.e14232 en eng HAL CCSD Elsevier info:eu-repo/semantics/altIdentifier/doi/10.1016/j.heliyon.2023.e14232 hal-04204000 https://hal.science/hal-04204000 doi:10.1016/j.heliyon.2023.e14232 ISSN: 2405-8440 Heliyon https://hal.science/hal-04204000 Heliyon, 2023, 9 (3), e14232 (17p.). ⟨10.1016/j.heliyon.2023.e14232⟩ [SDV]Life Sciences [q-bio] info:eu-repo/semantics/article Journal articles 2023 ftccsdartic https://doi.org/10.1016/j.heliyon.2023.e14232 2024-01-28T00:34:16Z We used ancient DNA (aDNA) extraction methods to sequence museum voucher samples of Oligobrachia webbi, a frenulate siboglinid polychaete described from a northern Norwegian fjord over fifty years ago. Our sequencing results indicate a genetic match with the cryptic seep species, Oligobrachia haakonmosbiensis (99% pairwise identity for 574 bp mtCOI fragments). Due to its similarity with O. webbi, the identity of O. haakonmosbiensis has been a matter of debate since its description, which we have now resolved. Furthermore, our results demonstrate that chemosynthesis-based siboglinids, that constitute the bulk of the biomass at Arctic seeps are not seep specialists. Our data on sediment geochemistry and carbon and nitrogen content reveal reduced conditions in fjords/sounds, similar to those at seep systems. Accumulation and decomposition of both terrestrial and marine organic matter results in the buildup of methane and sulfide that apparently can sustain chemosymbiotic fauna. The occurrence of fjords and by extension, highly reducing habitats, could have led to Arctic chemosymbiotic species being relatively generalist with their habitat, as opposed to being seep or vent specialists. Our stable isotope analyses indicate the incorporation of photosynthetically derived carbon in some individuals, which aligns with experiments conducted on frenulates before the discovery of chemosynthesis that demonstrated their ability to take up organic molecules from the surrounding sediment. Since reduced gases in non-seep environments are ultimately sourced from photosynthetic processes, we suggest that the extreme seasonality of the Arctic has resulted in Arctic chemosymbiotic animals seasonally changing their degree of reliance on chemosynthetic partners. Overall, the role of chemosynthesis in Arctic benthos and marine ecosystems and links to photosynthesis may be complex, and more extensive than currently known. Article in Journal/Newspaper Arctic Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) Arctic Heliyon 9 3 e14232
institution Open Polar
collection Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe)
op_collection_id ftccsdartic
language English
topic [SDV]Life Sciences [q-bio]
spellingShingle [SDV]Life Sciences [q-bio]
Sen, Arunima
Andersen, Liselotte W.
Kjeldsen, Kasper U.
Michel, Loïc
Hong, Wei Li
Choquet, Marvin
Rasmussen, Tine L.
The phylogeography and ecology of oligobrachia frenulate species suggest a generalist chemosynthesis-based fauna in the arctic
topic_facet [SDV]Life Sciences [q-bio]
description We used ancient DNA (aDNA) extraction methods to sequence museum voucher samples of Oligobrachia webbi, a frenulate siboglinid polychaete described from a northern Norwegian fjord over fifty years ago. Our sequencing results indicate a genetic match with the cryptic seep species, Oligobrachia haakonmosbiensis (99% pairwise identity for 574 bp mtCOI fragments). Due to its similarity with O. webbi, the identity of O. haakonmosbiensis has been a matter of debate since its description, which we have now resolved. Furthermore, our results demonstrate that chemosynthesis-based siboglinids, that constitute the bulk of the biomass at Arctic seeps are not seep specialists. Our data on sediment geochemistry and carbon and nitrogen content reveal reduced conditions in fjords/sounds, similar to those at seep systems. Accumulation and decomposition of both terrestrial and marine organic matter results in the buildup of methane and sulfide that apparently can sustain chemosymbiotic fauna. The occurrence of fjords and by extension, highly reducing habitats, could have led to Arctic chemosymbiotic species being relatively generalist with their habitat, as opposed to being seep or vent specialists. Our stable isotope analyses indicate the incorporation of photosynthetically derived carbon in some individuals, which aligns with experiments conducted on frenulates before the discovery of chemosynthesis that demonstrated their ability to take up organic molecules from the surrounding sediment. Since reduced gases in non-seep environments are ultimately sourced from photosynthetic processes, we suggest that the extreme seasonality of the Arctic has resulted in Arctic chemosymbiotic animals seasonally changing their degree of reliance on chemosynthetic partners. Overall, the role of chemosynthesis in Arctic benthos and marine ecosystems and links to photosynthesis may be complex, and more extensive than currently known.
author2 Biologie des Organismes et Ecosystèmes Aquatiques (BOREA)
Université de Caen Normandie (UNICAEN)
Normandie Université (NU)-Normandie Université (NU)-Muséum national d'Histoire naturelle (MNHN)-Institut de Recherche pour le Développement (IRD)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Université des Antilles (UA)
Biologie et Ecologie des Ecosystèmes Marins Profonds (BEEP)
Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)
format Article in Journal/Newspaper
author Sen, Arunima
Andersen, Liselotte W.
Kjeldsen, Kasper U.
Michel, Loïc
Hong, Wei Li
Choquet, Marvin
Rasmussen, Tine L.
author_facet Sen, Arunima
Andersen, Liselotte W.
Kjeldsen, Kasper U.
Michel, Loïc
Hong, Wei Li
Choquet, Marvin
Rasmussen, Tine L.
author_sort Sen, Arunima
title The phylogeography and ecology of oligobrachia frenulate species suggest a generalist chemosynthesis-based fauna in the arctic
title_short The phylogeography and ecology of oligobrachia frenulate species suggest a generalist chemosynthesis-based fauna in the arctic
title_full The phylogeography and ecology of oligobrachia frenulate species suggest a generalist chemosynthesis-based fauna in the arctic
title_fullStr The phylogeography and ecology of oligobrachia frenulate species suggest a generalist chemosynthesis-based fauna in the arctic
title_full_unstemmed The phylogeography and ecology of oligobrachia frenulate species suggest a generalist chemosynthesis-based fauna in the arctic
title_sort phylogeography and ecology of oligobrachia frenulate species suggest a generalist chemosynthesis-based fauna in the arctic
publisher HAL CCSD
publishDate 2023
url https://hal.science/hal-04204000
https://doi.org/10.1016/j.heliyon.2023.e14232
geographic Arctic
geographic_facet Arctic
genre Arctic
genre_facet Arctic
op_source ISSN: 2405-8440
Heliyon
https://hal.science/hal-04204000
Heliyon, 2023, 9 (3), e14232 (17p.). ⟨10.1016/j.heliyon.2023.e14232⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1016/j.heliyon.2023.e14232
hal-04204000
https://hal.science/hal-04204000
doi:10.1016/j.heliyon.2023.e14232
op_doi https://doi.org/10.1016/j.heliyon.2023.e14232
container_title Heliyon
container_volume 9
container_issue 3
container_start_page e14232
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